The B-cell leukemia/lymphoma-2 (bcl-2) gene is a protooncogene
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1 Expression of in Enteric Neurons in Normal Human Bowel and Hirschsprung Disease Tomas Wester, MD, PhD; Yngve Olsson, MD, PhD; Leif Olsen, MD, PhD Objective. The protein has the functional role of blocking apoptosis, ie, programmed cell death. This protein is widely expressed in the developing central and peripheral nervous systems. The purpose of this study was to map expression in the human enteric nervous system, as this has not previously been done. Methods. Rectal specimens were obtained at autopsy of 13 fetuses at 13 to 31 weeks of gestation. Normal colon was also obtained from 5 children and 2 adults, and, in addition, ganglionic and aganglionic bowel resected in 11 patients with Hirschsprung disease was examined. Specimens were fixed in formalin, embedded in paraffin, and analyzed with immunohistochemical methods, using antibodies raised against and neuron-specific enolase (). Results. The protein was expressed in myenteric and submucous ganglion cells in fetuses, children, and adults. Nerve fibers of the enteric plexuses that were bcl- 2 immunoreactive were few compared with the number of -immunoreactive nerve fibers. In aganglionic bowel no or -immunoreactive ganglion cells were revealed. Results of immunohistochemistry showed clearly stained hypertrophic nerve bundles, known to be of extrinsic origin, which were only weakly immunoreactive. Conclusion. Expression of in enteric ganglion cells of the myenteric and submucous plexuses is displayed in the fetus and during childhood and is also retained in adult bowel. Immunohistochemical analysis of provides a good marker for identification of ganglion cells in Hirschsprung disease and may also be valuable for the diagnosis of disorders characterized by hypoganglionosis or hyperganglionosis. (Arch Pathol Lab Med. 1999;123: ) The B-cell leukemia/lymphoma-2 () gene is a protooncogene first identified in studies of t(14;18) chromosome translocation in human follicular lymphoma. 1,2 The protein is localized in the inner mitochondria membranes. 3 Expression of is associated with cell development, maturation, and differentiation. 4 Furthermore, has been found to have the specific functional role of blocking programmed cell death, or apoptosis, 5 but the mechanism by which this effect is exerted is not known. 6 During the development of the normal nervous system, cell death takes place, resulting in a loss of 20% to 80% of all neurons. 7 The protein is widely expressed in the nervous system during development. However, in the central nervous system, immunoreactivity gradually declines with aging. On the other hand, expression is selectively retained in the adult peripheral nervous system, suggesting a role in neuronal survival. 8 Hirschsprung disease is characterized by the absence of ganglion cells in the distal hindgut. 9 The enteric neurons are derived from the vagal neural crest. 10 Neuroblasts migrate from the vagal neural crest in the craniocaudal direction and appear in the esophagus at 5 weeks gestation Accepted for publication June 3, From the Department of Paediatric Surgery, University Children s Hospital (Drs Wester and Olsen), and Laboratory of Neuropathology, Department of Genetics and Pathology, University Hospital (Dr Olsson), Uppsala, Sweden. Reprints: Tomas Wester, MD, PhD, Department of Paediatric Surgery, University Children s Hospital, S Uppsala, Sweden. and in the rectum at 12 weeks gestation. 11 In 1967, Okamoto and Ueda 11 hypothesized that aganglionosis may be the result of a migrational arrest, but development of normal enteric ganglia also requires differentiation and survival of the neuroblasts. Pachnis et al 12 examined the role of programmed cell death in the development of the enteric nervous system in RET mutant mouse embryos, which are aganglionic distal to the cardiac stomach. They found that the majority of the precursor cells of the enteric nervous system underwent apoptosis as they entered the foregut. The etiology of Hirschsprung disease remains unclear, but it may be hypothesized that aganglionosis occurs as a result of apoptosis of neuroblasts that results either from intrinsic abnormalities within these cells or from deficient signaling by mesenchymal cells along their migratory path. The role of protein in the enteric nervous system has not been clarified, and to our knowledge, there is no systematic description of expression in the human enteric nervous system. The purpose of this study was to characterize the immunoreactivity in the human fetal bowel and in bowel obtained at surgery in children and adults. Furthermore, bowel resected at definitive operation for Hirschsprung disease was examined to assess the usefulness of anti as an enteric neuronal marker. Anti neuron-specific enolase () was used as a reference marker for the neural component. The reason for this choice was that immunohistochemistry is a frequently used standard marker of enteric neurons, which has already been well defined in the human fetal bowel Arch Pathol Lab Med Vol 123, December 1999 Expression of Wester et al
2 MATERIALS AND METHODS Rectal specimens were obtained for diagnostic purposes at postmortem examination of 13 fetuses at 13 to 31 weeks of gestation. Autopsy was performed within 24 hours after death in most of the cases. Normal tissue from the sigmoid colon was taken on opening or closure of a colostomy in 5 patients, aged 1 day to 4 years 7 months (mean, 1 year 8 months), with anorectal malformations. Colonic specimens were also obtained at surgery in 2 adult patients, aged 78 and 87 years. The morphology of the bowel wall was normal in all these 20 cases at routine histopathologic examination of hematoxylin-eosin stained sections, although the mucosa showed autolytic alterations in the fetal postmortem cases. Furthermore, in 11 patients undergoing rectosigmoid resection for Hirschsprung disease at an age ranging from 13 months to 8 years 10 months (mean, 3 years 1 month), ganglionic and aganglionic bowel was investigated. The study was approved by the Ethics Committee of the Faculty of Medicine of Uppsala University. Tissue Preparation The specimens were fixed in 10% formalin overnight and embedded in paraffin. Sections 5 m thick were cut, placed on polylysine L coated slides, and incubated at 37C overnight. All sections were deparaffinized in xylene and hydrated. Immunohistochemistry Antigen retrieval by microwave oven heating was performed for both antibodies. The sections were boiled (750 W) in citric acid buffer (10 mm, ph 6.0) for 5 minutes () or 10 minutes (). The sections were allowed to cool to room temperature in the buffer and were then rinsed in phosphate-buffered saline (PBS ph 7.4). The endogenous peroxidase activity was blocked in 2% hydrogen peroxide in distilled water for 5 minutes, and the sections were then rinsed in PBS. Thereafter they were incubated with normal goat serum (Dako, Glostrup, Denmark, product number X0907, dilution 1:5) in PBS for 20 minutes at room temperature. Incubation with the primary antibody took place overnight at 4C () or for 1 hour at room temperature (). A further description of the primary antibodies is provided in Table 1. After rinsing in PBS, the slides were incubated with a biotinylated secondary antibody, goat anti-mouse (Dako, product number E0433, dilution 1:200) for 30 minutes at room temperature. The sections were then incubated in a kit for avidinbiotin complex method (Vectastain elite ABC kit, Vector Laboratories, Burlingame, Calif) for 30 minutes and developed in 3,3diaminobenzidine tetrahydrochloride (DAB, Sigma, London, England). Counterstaining with hematoxylin was performed. Finally, the sections were dehydrated, cleared in xylene, and mounted in water insoluble glue (Pertex, Histolab, Göteborg, Sweden). Immunoreactivity was absent in negative controls in which the primary antibody was omitted. The slides were analyzed by light microscopy. RESULTS Fetal Rectum Ganglion cells (Table 2) that were immunoreactive were distinguished at 13 weeks of gestation. These cells were mainly confined to the myenteric plexus, but scattered positive cells were also seen in the submucosa, forming the immature submucous plexus. Nerve axon fibers associated with the myenteric plexus were only weakly stained or did not stain at all (Figure, A). With increasing gestational age, up to 31 weeks of gestation, the appearance of the myenteric plexus did not undergo any changes. However, the submucous plexus became more organized, and at 20 to 22 weeks of gestation an inner and an outer submucous plexus could be distinguished. Epithelial cells that were immunoreactive were seen in the mucosal crypts, and strong immunoreactivity was observed in the peripheral part of lymph nodules. The immunohistochemistry revealed a distribution of ganglion cells similar to that shown by immunohistochemistry. On the other hand, the nerve axons within the myenteric ganglia were immunoreactive, which made it more difficult to distinguish the individual cell bodies compared with specimens stained with anti (Figure, B and Table 3). Normal Sigmoid Colon in Children In the cases involving children, was clearly expressed in the myenteric and submucous ganglion cells. As in the fetal cases, nerve fibers associated with the myenteric plexus stained weakly. A few well-stained nerve bundles were observed in the circular muscle layer. Immunoreactivity of in the mucosa was confined to epithelial cells in the crypt bases. Lymph nodules stained intensely, except for the germinal center. The distribution of -immunoreactive neurons was identical to that of cells labeled by anti. There were abundant -positive fibers in the circular muscle layer, in contrast to the few fibers reactive to. A few immunoreactive cell bodies were also seen in the circular muscle layer (Table 3). Adult Bowel Immunoreactivity of was displayed in myenteric and submucous ganglion cells. Occasional small immunoreactive cells were disclosed within the myenteric ganglia, representing small neurons or glial cells. As in childhood cases, few positive nerve bundles and occasional cell bodies were seen in the circular muscle layer (Figure, C). Epithelial cells in the crypt bases were weakly positive, whereas strong staining was seen in the lymphoid tissue (Table 3). Hirschsprung Disease In specimens of ganglionic bowel from patients with Hirschsprung disease, immunohistochemistry clearly disclosed the enteric neurons of the myenteric and submucous plexuses. However, immunoreactivity was weak in peripheral nerve bundles in the intermuscular space as well as in nerve fibers within the ganglia (Figure, E). In the circular muscle layer, a few clearly staining peripheral nerve bundles were revealed as well as occasional cell bodies. Epithelial cells in the crypt bases of the intestinal mucosa expressed. Furthermore, immunoreactivity was observed in submucosal lymphoid tissue. The distribution of the immunoreactivity was similar to that disclosed with immunohistochemistry, but nerve axons within the ganglia and nerve bundles of the plexus in the intermuscular space were strongly immunoreactive, and abundant peripheral nerve bundles were seen in the circular muscle layer (Figure, F and Table 3). In the aganglionic segment of the resected bowel no bcl- 2 immunoreactive ganglion cells were seen. Hypertrophic nerve bundles in the intermuscular space and in the submucosa stained only weakly (Figure, D). Lymphoid tissue in the submucosa and epithelial cells in the crypt bases stained as in the ganglionic bowel. No -immunoreactive cell bodies were observed in the aganglionic bowel, but the hypertrophic nerve trunks were clearly immunoreactive in the intermuscular space and in the submucosa (Table 3). Arch Pathol Lab Med Vol 123, December 1999 Expression of Wester et al 1265
3 A, At 14 weeks of gestation is clearly expressed in myenteric and submucous neurons (original magnification 100). B, Neuron-specific enolase () is also expressed at 14 weeks of gestation (original magnification 66). C, Expression of is retained in the adult enteric ganglion cells, as demonstrated in this case at 78 years of age (original magnification 66). D, An immunoreactive hypertrophic nerve bundle in the aganglionic segment of bowel in Hirschsprung disease (original magnification 50). E, In ganglionic bowel, resected in patients with Hirschsprung disease, is strongly expressed in the neuronal component (original magnification 50). F, In the ganglionic segment of bowel in Hirschsprung disease, is also strongly expressed. Axons within the myenteric ganglia stain stronger with immunohistochemistry compared with (original magnification 50). COMMENT Blocking programmed cell death is the functional role of. Our study demonstrates that is expressed in enteric neurons of the fetal gut and in the postnatal gut. The immunoreactivity is also retained in adult enteric neurons. These results indicate that the protein may be involved in promoting survival of the enteric neurons throughout life. The enteric nervous system can function independently of the central nervous system and has been described as the brain of the gut. 14 In this respect, the enteric nervous system differs from the rest of the peripheral nervous system. Furthermore, the enteric glial cells are closely related to astrocytes, found in the central nervous system. 15 However, despite these characteristics, the enteric nervous system is part of the peripheral nervous system Arch Pathol Lab Med Vol 123, December 1999 Expression of Wester et al
4 Table 1. Survey of the Antibodies Used* Antibody Clone/Product No. Characteristics Dilution 124/MO887 Monoclonal, mouse, antihuman BBS/NC/VI-H14 Monoclonal, mouse, antihuman 1:40 1:100 * Source of both antibodies is Dako, Glostrup, Denmark. indicates neuron-specific enolase. Term Ganglion cell Ganglion Nerve fiber Nerve bundle Table 2. Terminology Definition Neuron Cluster of ganglion cells and glial cells Nerve axon, for instance, within a ganglion Bundle of nerve fibers, for example, the internodal strands of the myenteric and submucous plexuses or the nerve bundles innervating the circular muscle layer of the bowel wall. The finding that expression is retained in the adult enteric nervous system is in line with the observation of expression in other parts of the peripheral nervous system in adults. On the other hand, immunoreactivity decreases in the central nervous system with aging, although it is present during development. 8 This difference may be related to the potential of the peripheral nervous system for regeneration. 8 It has been demonstrated that after transection and reanastomosis of the intestine, regeneration of the myenteric plexus occurs. 17,18 Expression of has been found in other cell types that are proliferating or have a long life span. For instance, protein is widely expressed in hematopoietic cell lines. 3 Lu et al 19 investigated the expression of protein in nonhematopoietic human embryonal and adult tissues. Regarding the adult gastrointestinal tract, they demonstrated protein in the basal colonic crypt cells but not in the stomach or small intestine. The authors briefly mention that expression was observed in neurons and Schwann cells in the 2 fetal cases at 16 weeks of gestation but make no comments on the adult cases. Hockenberry et al 5 also investigated the expression of protein in human tissues, including the gastrointestinal tract. Crypt cells that are immunoreactive were found in the colon and also in the small intestine, in contrast to the report by Lu et al. 19 Nothing is mentioned concerning the enteric nervous system by these 2 groups of investigators, who only described findings confined to the mucosa. Novack et al 20 investigated expression in the murine fetus but did not discuss the enteric nervous system. Previous studies have demonstrated that the myenteric and submucous plexuses are still developing postnatally. The neuron density decreases markedly with increasing age. 21,22 It is not clear, however, whether this decrease represents a reduction in the total number of enteric neurons, which could be explained by programmed cell death, or whether it is the result of bowel growth and thus an increasing bowel surface area. To our knowledge, the role of anti as a marker of enteric neurons has not previously been investigated. The staining properties of formalin-fixed tissue were consistently good, but antigen retrieval by boiling of the specimens in citric acid buffer in a microwave oven was necessary. Anti is particularly suitable for visualization of the nerve cell bodies, as the nerve fibers within the myenteric ganglia stain only weakly. This makes immunohistochemistry different from the use of standard neuronal markers such as anti-, 23 anti protein gene product 9.5, 24 NADPH-diaphorase histochemistry, 25 and acetylcholinesterase histochemistry, 26 all of which provide strong staining of nerve fibers. It also differs from anti S- 100, which is a specific marker for enteric glial cells. 27 Thus, immunostaining may be an option for neuron counting, which is important for the diagnosis of disorders characterized by hyperganglionosis or hypoganglionosis of the enteric plexuses. In Hirschsprung disease the aganglionic segment of the bowel showed no ganglion cells with use of anti and. The immunoreactivity in the hypertrophic nerve trunks in the intermuscular space and submucosa was weak in contrast to the distinct immunoreactivity. The expression disclosed in epithelial cells and lymphoid tissue was identical in Hirschsprung disease and normal bowel. The neuronal component of ganglionic bowel in specimens from patients with Hirschsprung disease appeared identical to that of the normal bowel specimens. In conclusion, protein is expressed in the enteric nervous system in the human fetus, at least from 13 weeks of gestation, and during childhood. Expression of is also retained in enteric ganglia in the adult bowel, which may indicate that is involved in promoting survival Table 3. Normal bowel Fetus Child Adult Hirschsprung disease Ganglionic Aganglionic Staining of the Neuronal Tissue in the Bowel Wall With Anti and Anti-* Ganglion Cells MP/SMP Nerve Fibers Within Ganglia or or or or Nerve Bundles Arch Pathol Lab Med Vol 123, December 1999 Expression of Wester et al 1267 or or or or or IM/SM or CM or * indicates neuron-specific enolase; MP, myenteric plexus; SMP, submucous plexus; IM, intermuscular space; SM, submucosa; and CM, circular muscle layer. Staining intensity was assessed as strong (), weak (), or absent (). A few well-stained fibers were observed. Occasional cell bodies were also seen. Hypertrophic nerve bundles of extrinsic origin.
5 of enteric neurons throughout life. In patients with Hirschsprung disease, we demonstrated that immunohistochemistry may serve as an additional marker for this diagnosis, and it may also be useful in disorders characterized by hyperganglionosis or hypoganglionosis. This work was supported by the HRH Crown Princess Louisa s Association for Child Medical Care. We are also grateful to Bengt Sandstedt who contributed specimens and to Maud Marsden for linguistic revision of the manuscript. References 1. Tsujimoto Y, Finger LR, Yunis J, Nowell PC, Croce CM. Cloning of the chromosome breakpoint of neoplastic B cells with the t(14;18) chromosome translocation. Science. 1984;226: Bakhshi A, Jensen JP, Goldman P, et al. Cloning the chromosomal breakpoint on t(14;18) human lymphomas: clustering around JH on chromosome 14 and near a transcriptional unit on 18. Cell. 1985;41: Hockenberry D, Nunez G, Milliman C, Schreiber RD, Korsmeyer SJ. Bcl-2 is an inner mitochondrial membrane protein that blocks programmed cell death. Nature. 1990;348: Korsmeyer SJ, McDonnell TJ, Nunez G, Hockenbery D, Young R. Bcl-2: B cell life, death and neoplasia. Curr Top Microbiol Immunol. 1990;166: Hockenberry DM, Zutter M, Hickey W, Nahm M, Korsmeyer SJ. BCL2 protein is topographically restricted in tissues characterized by apoptotic cell death. Proc Natl Acad Sci U S A. 1991;88: Merry DE, Korsmeyer SJ. Bcl-2 gene family in the nervous system. Annu Rev Neurosci. 1997;20: Oppenheim RW. Cell death during development of the nervous system. Annu Rev Neurosci. 1991;14: Merry DE, Veis DJ, Hickey WF, Korsmeyer SJ. protein expression is widespread in the developing nervous system and retained in the adult PNS. Development. 1994;120: Puri P. Hirschsprung s disease. In: Puri P, ed. Newborn Surgery. Oxford, England: Butterworth-Heinemann; 1996: Yntema CL, Hammond WS. The origin of intrinsic ganglia of trunk viscera from vagal neural crest in the chick embryo. J Comp Neurol. 1954;101: Okamoto E, Ueda T. Embryogenesis of intramural ganglia of the gut and its relation to Hirschsprung s disease. J Pediatr Surg. 1967;2: Pachnis V, Durbec P, Taraviras S, Grigoriou M, Natarajan D. Neural injury, repair, and adaptation in the GI tract III: role of the RET signal transduction pathway in development of the mammalian enteric nervous system. Am J Physiol. 1998;275:G183 G Fekete E, Benedeczky I, Timmermans J-P, Resch BA, Scheuermann DW. Sequential pattern of nerve-muscle contacts in the small intestine of developing human fetus: an ultrastructural and immunohistochemical study. Histol Histopathol. 1996;11: Goyal RK, Hirano I. The enteric nervous system. N Engl J Med. 1996;334: Jessen KR, Mirsky R. Astrocyte-like glia in the peripheral nervous system: an immunohistochemical study of the enteric glia. J Neurosci. 1983;3: Gershon MD, Kierschgessner AL, Wade PR. Functional anatomy of the enteric nervous system. In: Johnson LR, ed. Physiology of the Gastrointestinal Tract. New York, NY: Raven Press; 1994: Furness JB, Costa M. The Enteric Nervous System. New York, NY: Churchill Livingstone; Tokui K, Sakanaka M, Kimura S. Progressive reorganization of the myenteric plexus during one year following reanastomosis of the ileum of the guinea pig. Cell Tissue Res. 1994;277: Lu Q-L, Poulsom R, Wong L, Hanby AM. Bcl-2 expression in adult and embryonic non-haematopoietic tissues. J Pathol. 1993;169: Novack DV, Korsmeyer SJ. Bcl-2 protein expression during murine development. Am J Pathol. 1994;145: Wester T, OBriain DS, Puri P. Notable postnatal alterations in the myenteric plexus of normal human bowel. Gut. 1999;44: Wester T, O Briain DS, Puri P. Morphometric aspects of the submucous plexus in wholemount preparations of normal human distal colon. J Pediatr Surg. 1998;33: Frykberg T, Esscher T, Påhlman S, Olsson Y. Neuron-specific enolase as a marker for intestinal neurons. Acta Neuropathol. 1985;66: Sams VR, Bobrow LG, Happerfield L, Keeling J. Evaluation of PGP 9.5 in the diagnosis of Hirschsprung s disease. J Pathol. 1992;168: Scherer-Singler U, Vincent SR, Kimura H, McGeer EG. Demonstration of a unique population of neurons with NADPH-diaphorase histochemistry. J Neurosci Met. 1983;9: Karnovsky MJ, Roots L. A direct-colouring thiocholine method for cholinesterases. J Histochem Cytochem. 1964;12: Ferri G-L, Probert L, Cocchia D, Michetti F, Marangos PJ, Polak JM. Evidence of the presence of S-100 protein in the glial component of the human enteric nervous system. Nature. 1982;297: Arch Pathol Lab Med Vol 123, December 1999 Expression of Wester et al
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